CD47 Agonist Peptides Induce Programmed Cell Death in Refractory Chronic Lymphocytic Leukemia B Cells via PLCγ1 Activation: Evidence from Mice and Humans
In this study, Santos Susin and colleagues demonstrate that a serum-stable CD47 agonist peptide is highly effective at inducing apoptosis in chronic lymphocytic leukemia B-cells and mice.
Vyšlo v časopise:
CD47 Agonist Peptides Induce Programmed Cell Death in Refractory Chronic Lymphocytic Leukemia B Cells via PLCγ1 Activation: Evidence from Mice and Humans. PLoS Med 12(3): e32767. doi:10.1371/journal.pmed.1001796
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Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pmed.1001796
Souhrn
In this study, Santos Susin and colleagues demonstrate that a serum-stable CD47 agonist peptide is highly effective at inducing apoptosis in chronic lymphocytic leukemia B-cells and mice.
Zdroje
1. Chiorazzi N, Ferrarini M (2003) B cell chronic lymphocytic leukemia: lessons learned from studies of the B cell antigen receptor. Annu Rev Immunol 21: 841–894. 12615894
2. Dighiero G, Hamblin TJ (2008) Chronic lymphocytic leukaemia. Lancet 371: 1017–1029. doi: 10.1016/S0140-6736(08)60456-0 18358929
3. Pekarsky Y, Zanesi N, Croce CM (2010) Molecular basis of CLL. Semin Cancer Biol 20: 370–376. doi: 10.1016/j.semcancer.2010.09.003 20863894
4. Martin-Subero JI, Lopez-Otin C, Campo E (2013) Genetic and epigenetic basis of chronic lymphocytic leukemia. Curr Opin Hematol 20: 362–368. doi: 10.1097/MOH.0b013e32836235dc 23719185
5. Gaidano G, Foa R, Dalla-Favera R (2012) Molecular pathogenesis of chronic lymphocytic leukemia. J Clin Invest 122: 3432–3438. doi: 10.1172/JCI64101 23023714
6. Gribben JG (2010) How I treat CLL up front. Blood 115: 187–197. doi: 10.1182/blood-2009-08-207126 19850738
7. Dohner H, Stilgenbauer S, Benner A, Leupolt E, Krober A, et al. (2000) Genomic aberrations and survival in chronic lymphocytic leukemia. N Engl J Med 343: 1910–1916. 11136261
8. Byrd JC, Furman RR, Coutre SE, Flinn IW, Burger JA, et al. (2013) Targeting BTK with ibrutinib in relapsed chronic lymphocytic leukemia. N Engl J Med 369: 32–42. doi: 10.1056/NEJMoa1215637 23782158
9. Burger JA, Chiorazzi N (2013) B cell receptor signaling in chronic lymphocytic leukemia. Trends Immunol 34: 592–601. doi: 10.1016/j.it.2013.07.002 23928062
10. Gao AG, Lindberg FP, Finn MB, Blystone SD, Brown EJ, et al. (1996) Integrin-associated protein is a receptor for the C-terminal domain of thrombospondin. J Biol Chem 271: 21–24. 8550562
11. Hatherley D, Graham SC, Turner J, Harlos K, Stuart DI, et al. (2008) Paired receptor specificity explained by structures of signal regulatory proteins alone and complexed with CD47. Mol Cell 31: 266–277. doi: 10.1016/j.molcel.2008.05.026 18657508
12. Brown EJ, Frazier WA (2001) Integrin-associated protein (CD47) and its ligands. Trends Cell Biol 11: 130–135. 11306274
13. Sarfati M, Fortin G, Raymond M, Susin S (2008) CD47 in the immune response: role of thrombospondin and SIRP-alpha reverse signaling. Curr Drug Targets 9: 842–850. 18855618
14. Oldenborg PA (2013) CD47: A cell surface glycoprotein which regulates multiple functions of hematopoietic cells in health and disease. ISRN Hematol 2013: 614619. doi: 10.1155/2013/614619 23401787
15. Isenberg JS, Annis DS, Pendrak ML, Ptaszynska M, Frazier WA, et al. (2009) Differential interactions of thrombospondin-1, -2, and -4 with CD47 and effects on cGMP signaling and ischemic injury responses. J Biol Chem 284: 1116–1125. doi: 10.1074/jbc.M804860200 19004835
16. Floquet N, Dedieu S, Martiny L, Dauchez M, Perahia D (2008) Human thrombospondin’s (TSP-1) C-terminal domain opens to interact with the CD-47 receptor: a molecular modeling study. Arch Biochem Biophys 478: 103–109. doi: 10.1016/j.abb.2008.07.015 18675774
17. Kaur S, Soto-Pantoja DR, Stein EV, Liu C, Elkahloun AG, et al. (2013) Thrombospondin-1 signaling through CD47 inhibits self-renewal by regulating c-Myc and other stem cell transcription factors. Sci Rep 3: 1673. doi: 10.1038/srep01673 23591719
18. Chao MP, Alizadeh AA, Tang C, Myklebust JH, Varghese B, et al. (2010) Anti-CD47 antibody synergizes with rituximab to promote phagocytosis and eradicate non-Hodgkin lymphoma. Cell 142: 699–713. doi: 10.1016/j.cell.2010.07.044 20813259
19. Zhao XW, Matlung HL, Kuijpers TW, van den Berg TK (2012) On the mechanism of CD47 targeting in cancer. Proc Natl Acad Sci U S A 109: E2843. doi: 10.1073/pnas.1209265109 22923695
20. Chao MP, Weissman IL, Majeti R (2012) The CD47-SIRPα pathway in cancer immune evasion and potential therapeutic implications. Curr Opin Immunol 24: 225–232. doi: 10.1016/j.coi.2012.01.010 22310103
21. Soto-Pantoja DR, Ridnour LA, Wink DA, Roberts DD (2013) Blockade of CD47 increases survival of mice exposed to lethal total body irradiation. Sci Rep 3: 1038. doi: 10.1038/srep01038 23301159
22. Weiskopf K, Ring AM, Ho CC, Volkmer JP, Levin AM, et al. (2013) Engineered SIRPα variants as immunotherapeutic adjuvants to anticancer antibodies. Science 341: 88–91. doi: 10.1126/science.1238856 23722425
23. Mateo V, Lagneaux L, Bron D, Biron G, Armant M, et al. (1999) CD47 ligation induces caspase-independent cell death in chronic lymphocytic leukemia. Nat Med 5: 1277–1284. 10545994
24. Merle-Beral H, Barbier S, Roue G, Bras M, Sarfati M, et al. (2009) Caspase-independent type III PCD: a new means to modulate cell death in chronic lymphocytic leukemia. Leukemia 23: 974–977. doi: 10.1038/leu.2008.321 19005478
25. Saumet A, Slimane MB, Lanotte M, Lawler J, Dubernard V (2005) Type 3 repeat/C-terminal domain of thrombospondin-1 triggers caspase-independent cell death through CD47/alphavbeta3 in promyelocytic leukemia NB4 cells. Blood 106: 658–667. 15784731
26. Majeti R, Chao MP, Alizadeh AA, Pang WW, Jaiswal S, et al. (2009) CD47 is an adverse prognostic factor and therapeutic antibody target on human acute myeloid leukemia stem cells. Cell 138: 286–299. doi: 10.1016/j.cell.2009.05.045 19632179
27. Sagawa M, Shimizu T, Fukushima N, Kinoshita Y, Ohizumi I, et al. (2011) A new disulfide-linked dimer of a single-chain antibody fragment against human CD47 induces apoptosis in lymphoid malignant cells via the hypoxia inducible factor-1α pathway. Cancer Sci 102: 1208–1215. doi: 10.1111/j.1349-7006.2011.01925.x 21401803
28. Pettersen RD, Hestdal K, Olafsen MK, Lie SO, Lindberg FP (1999) CD47 signals T cell death. J Immunol 162: 7031–7040. 10358145
29. Kosfeld MD, Frazier WA (1993) Identification of a new cell adhesion motif in two homologous peptides from the COOH-terminal cell binding domain of human thrombospondin. J Biol Chem 268: 8808–8814. 8473325
30. Gao AG, Frazier WA (1994) Identification of a receptor candidate for the carboxyl-terminal cell binding domain of thrombospondins. J Biol Chem 269: 29650–29657. 7525586
31. Burger P, Hilarius-Stokman P, de Korte D, van den Berg TK, van Bruggen R (2012) CD47 functions as a molecular switch for erythrocyte phagocytosis. Blood 119: 5512–5521. doi: 10.1182/blood-2011-10-386805 22427202
32. Kalas W, Swiderek E, Switalska M, Wietrzyk J, Rak J, et al. (2013) Thrombospondin-1 receptor mediates autophagy of RAS-expressing cancer cells and triggers tumour growth inhibition. Anticancer Res 33: 1429–1438. 23564783
33. Miyata Y, Watanabe S, Kanetake H, Sakai H (2012) Thrombospondin-1-derived 4N1K peptide expression is negatively associated with malignant aggressiveness and prognosis in urothelial carcinoma of the upper urinary tract. BMC Cancer 12: 372. doi: 10.1186/1471-2407-12-372 22928942
34. Manna PP, Frazier WA (2003) The mechanism of CD47-dependent killing of T cells: heterotrimeric Gi-dependent inhibition of protein kinase A. J Immunol 170: 3544–3553. 12646616
35. Manna PP, Frazier WA (2004) CD47 mediates killing of breast tumor cells via Gi-dependent inhibition of protein kinase A. Cancer Res 64: 1026–1036. 14871834
36. Johansson U, Higginbottom K, Londei M (2004) CD47 ligation induces a rapid caspase-independent apoptosis-like cell death in human monocytes and dendritic cells. Scand J Immunol 59: 40–49. 14723620
37. Johansson U, Londei M (2004) Ligation of CD47 during monocyte differentiation into dendritic cells results in reduced capacity for interleukin-12 production. Scand J Immunol 59: 50–57. 14723621
38. Sun L (2013) Peptide-based drug development. Mod Chem Appl 1: e103.
39. Le Garff-Tavernier M, Blons H, Nguyen-Khac F, Pannetier M, Brissard M, et al. (2011) Functional assessment of p53 in chronic lymphocytic leukemia. Blood Cancer J 1: e5. doi: 10.1038/bcj.2011.3 22829111
40. Van VQ, Baba N, Rubio M, Wakahara K, Panzini B, et al. (2012) CD47(low) status on CD4 effectors is necessary for the contraction/resolution of the immune response in humans and mice. PLoS ONE 7: e41972. doi: 10.1371/journal.pone.0041972 22870271
41. Raymond M, Rubio M, Fortin G, Shalaby KH, Hammad H, et al. (2009) Selective control of SIRP-alpha-positive airway dendritic cell trafficking through CD47 is critical for the development of T(H)2-mediated allergic inflammation. J Allergy Clin Immunol 124: 1333–1342. doi: 10.1016/j.jaci.2009.07.021 19748659
42. Barbet G, Demion M, Moura IC, Serafini N, Leger T, et al. (2008) The calcium-activated nonselective cation channel TRPM4 is essential for the migration but not the maturation of dendritic cells. Nat Immunol 9: 1148–1156. doi: 10.1038/ni.1648 18758465
43. Serafini N, Dahdah A, Barbet G, Demion M, Attout T, et al. (2012) The TRPM4 channel controls monocyte and macrophage, but not neutrophil, function for survival in sepsis. J Immunol 189: 3689–3699. 22933633
44. Beillard E, Pallisgaard N, van der Velden VH, Bi W, Dee R, et al. (2003) Evaluation of candidate control genes for diagnosis and residual disease detection in leukemic patients using ‘real-time’ quantitative reverse-transcriptase polymerase chain reaction (RQ-PCR)—a Europe Against Cancer program. Leukemia 17: 2474–2486. 14562124
45. Trinquet E, Fink M, Bazin H, Grillet F, Maurin F, et al. (2006) D-myo-inositol 1-phosphate as a surrogate of D-myo-inositol 1,4,5-tris phosphate to monitor G protein-coupled receptor activation. Anal Biochem 358: 126–135. 16965760
46. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG (2010) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 8: e1000412. doi: 10.1371/journal.pbio.1000412 20613859
47. O’Neil RG, Wu L, Mullani N (2005) Uptake of a fluorescent deoxyglucose analog (2-NBDG) in tumor cells. Mol Imaging Biol 7: 388–392. 16284704
48. Sick E, Niederhoffer N, Takeda K, Landry Y, Gies JP (2009) Activation of CD47 receptors causes histamine secretion from mast cells. Cell Mol Life Sci 66: 1271–1282. doi: 10.1007/s00018-009-8778-2 19205621
49. Powell MF, Stewart T, Otvos L Jr, Urge L, Gaeta FC, et al. (1993) Peptide stability in drug development. II. Effect of single amino acid substitution and glycosylation on peptide reactivity in human serum. Pharm Res 10: 1268–1273. 8234161
50. McDonald JF, Dimitry JM, Frazier WA (2003) An amyloid-like C-terminal domain of thrombospondin-1 displays CD47 agonist activity requiring both VVM motifs. Biochemistry 42: 10001–10011. 12924949
51. Hu M, Polyak K (2008) Microenvironmental regulation of cancer development. Curr Opin Genet Dev 18: 27–34. doi: 10.1016/j.gde.2007.12.006 18282701
52. Zhang W, Trachootham D, Liu J, Chen G, Pelicano H, et al. (2012) Stromal control of cystine metabolism promotes cancer cell survival in chronic lymphocytic leukaemia. Nat Cell Biol 14: 276–286. doi: 10.1038/ncb2432 22344033
53. Gardai SJ, McPhillips KA, Frasch SC, Janssen WJ, Starefeldt A, et al. (2005) Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 123: 321–334. 16239148
54. Chao MP, Jaiswal S, Weissman-Tsukamoto R, Alizadeh AA, Gentles AJ, et al. (2010) Calreticulin is the dominant pro-phagocytic signal on multiple human cancers and is counterbalanced by CD47. Sci Transl Med 2: 63ra94. doi: 10.1126/scitranslmed.3001375 21178137
55. Bras M, Yuste VJ, Roue G, Barbier S, Sancho P, et al. (2007) Drp1 mediates caspase-independent type III cell death in normal and leukemic cells. Mol Cell Biol 27: 7073–7088. 17682056
56. Barbier S, Chatre L, Bras M, Sancho P, Roue G, et al. (2009) Caspase-independent type III programmed cell death in chronic lymphocytic leukemia: the key role of the F-actin cytoskeleton. Haematologica 94: 507–517. doi: 10.3324/haematol.13690 19278964
57. Hirshman CA, Zhu D, Pertel T, Panettieri RA, Emala CW (2005) Isoproterenol induces actin depolymerization in human airway smooth muscle cells via activation of an Src kinase and GS. Am J Physiol Lung Cell Mol Physiol 288: L924–L931. 15821021
58. Danial NN, Korsmeyer SJ (2004) Cell death: critical control points. Cell 116: 205–219. 14744432
59. Feske S (2007) Calcium signalling in lymphocyte activation and disease. Nat Rev Immunol 7: 690–702. 17703229
60. Scharenberg AM, Humphries LA, Rawlings DJ (2007) Calcium signalling and cell-fate choice in B cells. Nat Rev Immunol 7: 778–789. 17853903
61. Giorgi C, Baldassari F, Bononi A, Bonora M, De Marchi E, et al. (2012) Mitochondrial Ca(2+) and apoptosis. Cell Calcium 52: 36–43. doi: 10.1016/j.ceca.2012.02.008 22480931
62. Poulin B, Sekiya F, Rhee SG (2005) Intramolecular interaction between phosphorylated tyrosine-783 and the C-terminal Src homology 2 domain activates phospholipase C-gamma1. Proc Natl Acad Sci U S A 102: 4276–4281. 15764700
63. Bertilaccio MT, Scielzo C, Simonetti G, Ponzoni M, Apollonio B, et al. (2010) A novel Rag2-/-gammac-/—xenograft model of human CLL. Blood 115: 1605–1609. doi: 10.1182/blood-2009-05-223586 20018917
64. Soto-Pantoja DR, Stein EV, Rogers NM, Sharifi-Sanjani M, Isenberg JS, et al. (2013) Therapeutic opportunities for targeting the ubiquitous cell surface receptor CD47. Expert Opin Ther Targets 17: 89–103. doi: 10.1517/14728222.2013.733699 23101472
65. Zhao XW, van Beek EM, Schornagel K, Van der Maaden H, Van Houdt M, et al. (2011) CD47-signal regulatory protein-α (SIRPα) interactions form a barrier for antibody-mediated tumor cell destruction. Proc Natl Acad Sci U S A 108: 18342–18347. doi: 10.1073/pnas.1106550108 22042861
66. Willingham SB, Volkmer JP, Gentles AJ, Sahoo D, Dalerba P, et al. (2012) The CD47-signal regulatory protein alpha (SIRPa) interaction is a therapeutic target for human solid tumors. Proc Natl Acad Sci U S A 109: 6662–6667. doi: 10.1073/pnas.1121623109 22451913
67. Jaiswal S, Jamieson CH, Pang WW, Park CY, Chao MP, et al. (2009) CD47 is upregulated on circulating hematopoietic stem cells and leukemia cells to avoid phagocytosis. Cell 138: 271–285. doi: 10.1016/j.cell.2009.05.046 19632178
68. Lax R (2010) The future of peptide development in the pharmaceutical industry. Pharmanuf Int Pept Rev 2: 10–15.
69. Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, et al. (2009) Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ 16: 3–11. doi: 10.1038/cdd.2008.150 18846107
70. Moubarak RS, Yuste VJ, Artus C, Bouharrour A, Greer PA, et al. (2007) Sequential activation of poly(ADP-ribose) polymerase 1, calpains, and Bax is essential in apoptosis-inducing factor-mediated programmed necrosis. Mol Cell Biol 27: 4844–4862. 17470554
71. Mateo V, Brown EJ, Biron G, Rubio M, Fischer A, et al. (2002) Mechanisms of CD47-induced caspase-independent cell death in normal and leukemic cells: link between phosphatidylserine exposure and cytoskeleton organization. Blood 100: 2882–2890. 12351399
72. Hogan PG, Lewis RS, Rao A (2010) Molecular basis of calcium signaling in lymphocytes: STIM and ORAI. Annu Rev Immunol 28: 491–533. doi: 10.1146/annurev.immunol.021908.132550 20307213
73. Parekh AB, Putney JW Jr (2005) Store-operated calcium channels. Physiol Rev 85: 757–810. 15788710
74. Wozniak AL, Wang X, Stieren ES, Scarbrough SG, Elferink CJ, et al. (2006) Requirement of biphasic calcium release from the endoplasmic reticulum for Fas-mediated apoptosis. J Cell Biol 175: 709–714. 17130290
75. Wilde JI, Watson SP (2001) Regulation of phospholipase C gamma isoforms in haematopoietic cells: why one, not the other? Cell Signal 13: 691–701. 11602179
76. Wang D, Feng J, Wen R, Marine JC, Sangster MY, et al. (2000) Phospholipase Cgamma2 is essential in the functions of B cell and several Fc receptors. Immunity 13: 25–35. 10933392
77. Le Roy C, Deglesne PA, Chevallier N, Beitar T, Eclache V, et al. (2012) The degree of BCR and NFAT activation predicts clinical outcomes in chronic lymphocytic leukemia. Blood 120: 356–365. doi: 10.1182/blood-2011-12-397158 22613791
78. Buchner M, Fuchs S, Prinz G, Pfeifer D, Bartholome K, et al. (2009) Spleen tyrosine kinase is overexpressed and represents a potential therapeutic target in chronic lymphocytic leukemia. Cancer Res 69: 5424–5432. doi: 10.1158/0008-5472.CAN-08-4252 19549911
79. Fujimoto TT, Katsutani S, Shimomura T, Fujimura K (2003) Thrombospondin-bound integrin-associated protein (CD47) physically and functionally modifies integrin alphaIIbbeta3 by its extracellular domain. J Biol Chem 278: 26655–26665. 12736272
80. Chung J, Gao AG, Frazier WA (1997) Thrombspondin acts via integrin-associated protein to activate the platelet integrin alphaIIbbeta3. J Biol Chem 272: 14740–14746. 9169439
81. Thompson CB (1995) Apoptosis in the pathogenesis and treatment of disease. Science 267: 1456–1462. 7878464
82. Parker JL, Newstead S (2014) Molecular basis of nitrate uptake by the plant nitrate transporter NRT1.1. Nature 507: 68–72. doi: 10.1038/nature13116 24572366
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